Flotillins functionally organize the bacterial membrane

Molecular Microbiology

Volumn 88, Issue 6, 2013, Pages 1205-1217

  Bach, Juri Niño ^a   Bramkamp, Marc ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FLOTILLIN; MEMBRANE PROTEIN; PENICILLIN BINDING PROTEIN 5; PROTEIN ACSA; PROTEIN ATPD; PROTEIN ATPG; PROTEIN FHUD; PROTEIN FTSH; PROTEIN FTSX; PROTEIN GLTT; PROTEIN GTAB; PROTEIN MNTA; PROTEIN NAG; PROTEIN OPPA; PROTEIN OPUAC; PROTEIN PTSL; PROTEIN QOXA; PROTEIN RBSB; PROTEIN RESC; PROTEIN SDHA; PROTEIN TAGU; PROTEIN YCLQ; PROTEIN YFIY; PROTEIN YHFQ; PROTEIN YUAG; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL MEMBRANE; CELL HETEROGENEITY; CELL METABOLISM; CONTROLLED STUDY; ENERGY METABOLISM; IN VIVO STUDY; INTRACELLULAR SIGNALING; MEMBRANE FLUIDITY; MEMBRANE FORMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN TRANSPORT; SEGREGATION ANALYSIS;

BACILLUS SUBTILIS; CELL MEMBRANE; MEMBRANE FLUIDITY; MEMBRANE MICRODOMAINS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MODELS, MOLECULAR;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

EID: 84879030282     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12252     Document Type: Article

References (76)

1. Almeida, P.F. (2009) Thermodynamics of lipid interactions in complex bilayers. Biochim Biophys Acta 1788: 72-85.
2. Atrih, A., Bacher, G., Allmaier, G., Williamson, M., and Foster, S.J. (1999) Analysis of peptidoglycan structure from vegetative cells of Bacillus subtilis 168 and role of PBP 5 in peptidoglycan maturation. J Bacteriol 181: 3956-3966.
3. Banning, A., Tomasovic, A., and Tikkanen, R. (2011) Functional aspects of membrane association of reggie/flotillin proteins. Curr Protein Pept Sci 12: 725-735.
4. Barak, I., Muchova, K., Wilkinson, A.J., O'Toole, P.J., and Pavlendova, N. (2008) Lipid spirals in Bacillus subtilis and their role in cell division. Mol Microbiol 68: 1315-1327.
5. Bickel, P.E., Scherer, P.E., Schnitzer, J.E., Oh, P., Lisanti, M.P., and Lodish, H.F. (1997) Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J Biol Chem 272: 13793-13802.
6. Bogdanov, M., and Dowhan, W. (2012) Lipid-dependent generation of dual topology for a membrane protein. J Biol Chem 287: 37939-37948.
7. Bramkamp, M., Weston, L., Daniel, R.A., and Errington, J. (2006) Regulated intramembrane proteolysis of FtsL protein and the control of cell division in Bacillus subtilis. Mol Microbiol 62: 580-591.
8. Branda, S.S., Chu, F., Kearns, D.B., Losick, R., and Kolter, R. (2006) A major protein component of the Bacillus subtilis biofilm matrix. Mol Microbiol 59: 1229-1238.
9. Browman, D.T., Hoegg, M.B., and Robbins, S.M. (2007) The SPFH domain-containing proteins: more than lipid raft markers. Trends Cell Biol 17: 394-402.
10. Brown, M.S., and Goldstein, J.L. (1997) The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89: 331-340.
11. Bürmann, F., Ebert, N., van Baarle, S., and Bramkamp, M. (2011) A bacterial dynamin-like protein mediating nucleotide-independent membrane fusion. Mol Microbiol 79: 1294-1304.
12. Campo, N., Tjalsma, H., Buist, G., Stepniak, D., Meijer, M., Veenhuis, M., etal. (2004) Subcellular sites for bacterial protein export. Mol Microbiol 53: 1583-1599.
13. Cybulski, L.E., and de Mendoza, D. (2011) Bilayer hydrophobic thickness and integral membrane protein function. Curr Protein Pept Sci 12: 760-766.
14. Dinic, J., Biverstahl, H., Maler, L., and Parmryd, I. (2011) Laurdan and di-4-ANEPPDHQ do not respond to membrane-inserted peptides and are good probes for lipid packing. Biochim Biophys Acta 1808: 298-306.
15. Doherty, G.J., and McMahon, H.T. (2009) Mechanisms of endocytosis. Annu Rev Biochem 78: 857-902.
16. Donovan, C., and Bramkamp, M. (2009) Characterization and subcellular localization of a bacterial flotillin homologue. Microbiology 155: 1786-1799.
17. Driessen, A.J., and Nouwen, N. (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77: 643-667.
18. Epand, R.M., and Epand, R.F. (2009) Lipid domains in bacterial membranes and the action of antimicrobial agents. Biochim Biophys Acta 1788: 289-294.
19. Fishov, I., and Norris, V. (2012) Membrane heterogeneity created by transertion is a global regulator in bacteria. Curr Opin Microbiol 15: 724-730.
20. Frick, M., Bright, N.A., Riento, K., Bray, A., Merrified, C., and Nichols, B.J. (2007) Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol 17: 1151-1156.
21. Garcia-Saez, A.J., and Schwille, P. (2010) Stability of lipid domains. FEBS Lett 584: 1653-1658.
22. Gaus, K., Zech, T., and Harder, T. (2006) Visualizing membrane microdomains by Laurdan 2-photon microscopy. Mol Membr Biol 23: 41-48.
23. Glebov, O.O., Bright, N.A., and Nichols, B.J. (2006) Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol 8: 46-54.
24. Hansen, C.G., and Nichols, B.J. (2009) Molecular mechanisms of clathrin-independent endocytosis. J Cell Sci 122: 1713-1721.
25. Hendrick, J.P., and Wickner, W. (1991) SecA protein needs both acidic phospholipids and SecY/E protein for functional high-affinity binding to the Escherichia coli plasma membrane. J Biol Chem 266: 24596-24600.
26. de Jong, I.G., Beilharz, K., Kuipers, O., and Veening, J.W. (2011) Live cell imaging of Bacillus subtilis and Streptococcus pneumoniae using automated time-lapse microscopy. J Vis Exp 53. doi:pii: 3145. 10.3791/3145
27. Kaiser, H.J., Lingwood, D., Levental, I., Sampaio, J.L., Kalvodova, L., Rajendran, L., and Simons, K. (2009) Order of lipid phases in model and plasma membranes. Proc Natl Acad Sci USA 106: 16645-16650.
28. Kaiser, H.J., Surma, M.A., Mayer, F., Levental, I., Grzybek, M., Klemm, R.W., etal. (2011) Molecular convergence of bacterial and eukaryotic surface order. J Biol Chem 286: 40631-40637.
29. Kawai, Y., Marles-Wright, J., Cleverley, R.M., Emmins, R., Ishikawa, S., Kuwano, M., etal. (2011) A widespread family of bacterial cell wall assembly proteins. EMBO J. 30: 4931-4941.
30. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
31. Langhorst, M.F., Reuter, A., and Stuermer, C.A. (2005) Scaffolding microdomains and beyond: the function of reggie/flotillin proteins. Cell Mol Life Sci 62: 2228-2240.
32. Langhorst, M.F., Solis, G., Hannbeck, S., Plattner, H., and Stuermer, C.A. (2007) Linking membrane microdomains to the cytoskeleton: regulation of the lateral mobility of reggie-1/flotillin-2 by interaction with actin. FEBS Lett 581: 4697-4703.
33. Lee, A.G. (1998) How lipids interact with an intrinsic membrane protein: the case of the calcium pump. Biochim Biophys Acta 1376: 381-390.
34. Lee, A.G. (2003) Lipid-protein interactions in biological membranes: a structural perspective. Biochim Biophys Acta 1612: 1-40.
35. Levental, I., Byfield, F.J., Chowdhury, P., Gai, F., Baumgart, T., and Janmey, P.A. (2009) Cholesterol-dependent phase separation in cell-derived giant plasma-membrane vesicles. Biochem J 424: 163-167.
36. Lingwood, D., and Simons, K. (2010) Lipid rafts as a membrane-organizing principle. Science 327: 46-50.
37. Lingwood, D., Kaiser, H.J., Levental, I., and Simons, K. (2009) Lipid rafts as functional heterogeneity in cell membranes. Biochem Soc Trans 37: 955-960.
38. Lonhienne, T.G., Sagulenko, E., Webb, R.I., Lee, K.C., Franke, J., Devos, D.P., etal. (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci USA 107: 12883-12888.
39. Lopez, C.S., Garda, H.A., and Rivas, E.A. (2002) The effect of osmotic stress on the biophysical behavior of the Bacillus subtilis membrane studied by dynamic and steady-state fluorescence anisotropy. Arch Biochem Biophys 408: 220-228.
40. Lopez, D., and Kolter, R. (2010) Functional microdomains in bacterial membranes. Genes Dev 24: 1893-1902.
41. Mall, S., Broadbridge, R., Sharma, R., Lee, A.G., and East, J.M. (2000) Effects of aromatic residues at the ends of transmembrane alpha-helices on helix interactions with lipid bilayers. Biochemistry 39: 2071-2078.
42. Matsumoto, K., Kusaka, J., Nishibori, A., and Hara, H. (2006) Lipid domains in bacterial membranes. Mol Microbiol 61: 1110-1117.
43. Mercier, R., Dominguez-Cuevas, P., and Errington, J. (2012) Crucial role for membrane fluidity in proliferation of primitive cells. Cell Rep 1: 417-423.
44. Mileykovskaya, E., and Dowhan, W. (2009) Cardiolipin membrane domains in prokaryotes and eukaryotes. Biochim Biophys Acta 1788: 2084-2091.
45. Mileykovskaya, E., Fishov, I., Fu, X., Corbin, B.D., Margolin, W., and Dowhan, W. (2003) Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo. J Biol Chem 278: 22193-22198.
46. Morrow, I.C., and Parton, R.G. (2005) Flotillins and the PHB domain protein family: rafts, worms and anaesthetics. Traffic 6: 725-740.
47. Nishibori, A., Kusaka, J., Hara, H., Umeda, M., and Matsumoto, K. (2005) Phosphatidylethanolamine domains and localization of phospholipid synthases in Bacillus subtilis membranes. J Bacteriol 187: 2163-2174.
48. Owen, D.M., Magenau, A., Williamson, D., and Gaus, K. (2012) The lipid raft hypothesis revisited - new insights on raft composition and function from super-resolution fluorescence microscopy. Bioessays 34: 739-747.
49. Partridge, S.R., and Errington, J. (1993) The importance of morphological events and intercellular interactions in the regulation of prespore-specific gene expression during sporulation in Bacillus subtilis. Mol Microbiol 8: 945-955.
50. Pike, L.J. (2006) Rafts defined: a report on the keystone symposium on lipid rafts and cell function. J Lipid Res 47: 1597-1598.
51. Rapoport, T.A. (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450: 663-669.
52. Rivera-Milla, E., Stuermer, C.A., and Malaga-Trillo, E. (2006) Ancient origin of reggie (flotillin), reggie-like, and other lipid-raft proteins: convergent evolution of the SPFH domain. Cell Mol Life Sci 63: 343-357.
53. Romantsov, T., Helbig, S., Culham, D.E., Gill, C., Stalker, L., and Wood, J.M. (2007) Cardiolipin promotes polar localization of osmosensory transporter ProP in Escherichia coli. Mol Microbiol 64: 1455-1465.
54. Romero, D., Aguilar, C., Losick, R., and Kolter, R. (2010) Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci USA 107: 2230-2234.
55. Saenz, J.P., Sezgin, E., Schwille, P., and Simons, K. (2012) Functional convergence of hopanoids and sterols in membrane ordering. Proc Natl Acad Sci USA 109: 14236-14240.
56. Schaffner, W., and Weissmann, C. (1973) A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal Biochem 56: 502-514.
57. Scheffers, D.J., Jones, L.J., and Errington, J. (2004) Several distinct localization patterns for penicillin-binding proteins in Bacillus subtilis. Mol Microbiol 51: 749-764.
58. Schmidt, K.L., Peterson, N.D., Kustusch, R.J., Wissel, M.C., Graham, B., Phillips, G.J., and Weiss, D.S. (2004) A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli. J Bacteriol 186: 785-793.
59. Schöbel, S., Zellmeier, S., Schumann, W., and Wiegert, T. (2004) The Bacillus subtilis σW anti-sigma factor RsiW is degraded by intramembrane proteolysis through YluC. Mol Microbiol 52: 1091-1105.
60. Simons, K., and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387: 569-572.
61. Simons, K., and Vaz, W.L. (2004) Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33: 269-295.
62. Singer, S.J., and Nicolson, G.L. (1972) The fluid mosaic model of the structure of cell membranes. Science 175: 720-731.
63. Slaughter, N., Laux, I., Tu, X., Whitelegge, J., Zhu, X., Effros, R., etal. (2003) The flotillins are integral membrane proteins in lipid rafts that contain TCR-associated signaling components: implications for T-cell activation. Clin Immunol 108: 138-151.
64. Solis, G.P., Hoegg, M., Munderloh, C., Schrock, Y., Malaga-Trillo, E., Rivera-Milla, E., and Stuermer, C.A. (2007) Reggie/flotillin proteins are organized into stable tetramers in membrane microdomains. Biochem J 403: 313-322.
65. Solomon, S., Masilamani, M., Rajendran, L., Bastmeyer, M., Stuermer, C.A., and Illges, H. (2002) The lipid raft microdomain-associated protein reggie-1/flotillin-2 is expressed in human B cells and localized at the plasma membrane and centrosome in PBMCs. Immunobiology 205: 108-119.
66. Spira, F., Mueller, N.S., Beck, G., von Olshausen, P., Beig, J., and Wedlich-Söldner, R. (2012) Patchwork organization of the yeast plasma membrane into numerous coexisting domains. Nat Cell Biol 14: 640-648.
67. Stuermer, C.A. (2010) The reggie/flotillin connection to growth. Trends Cell Biol 20: 6-13.
68. Tatsuta, T., Model, K., and Langer, T. (2005) Formation of membrane-bound ring complexes by prohibitins in mitochondria. Mol Biol Cell 16: 248-259.
69. Todd, J.A., Bone, E.J., and Ellar, D.J. (1985) The sporulation-specific penicillin-binding protein 5a from Bacillus subtilis is a DD-carboxypeptidase in vitro. Biochem J 230: 825-828.
70. Vanounou, S., Pines, D., Pines, E., Parola, A.H., and Fishov, I. (2002) Coexistence of domains with distinct order and polarity in fluid bacterial membranes. Photochem Photobiol 76: 1-11.
71. Veenendaal, A.K., van der Does, C., and Driessen, A.J. (2004) The protein-conducting channel SecYEG. Biochim Biophys Acta 1694: 81-95.
72. Wadenpohl, I., and Bramkamp, M. (2010) DivIC stabilizes FtsL against RasP cleavage. J Bacteriol 192: 5260-5263.
73. Wehrl, W., Niederweis, M., and Schumann, W. (2000) The FtsH protein accumulates at the septum of Bacillus subtilis during cell division and sporulation. J Bacteriol 182: 3870-3873.
74. Wheeler, G., and Tyler, K.M. (2011) Widefield microscopy for live imaging of lipid domains and membrane dynamics. Biochim Biophys Acta 1808: 634-641.
75. Wittig, I., Braun, H., and Schagger, H. (2006) Blue native PAGE. Nat Protoc 1: 418-428.
76. Yepes, A., Schneider, J., Mielich, B., Koch, G., Garcia-Betancur, J.C., Ramamurthi, K.S., etal. (2012) The biofilm formation defect of a Bacillus subtilis flotillin-defective mutant involves the protease FtsH. Mol Microbiol 86: 457-471.